Allochthonous dissolved organic matter controls bacterial carbon production in old-growth and clearfelled headwater streams

Freshwater Science

Volumn 32, Issue 3, 2013, Pages 821-836

  Burrows, Ryan M ^a,b   Fellman, Jason B ^c   Magierowski, Regina H ^a   Barmuta, Leon A ^a,b  

^a UNIVERSITY OF TASMANIA   (Australia)

^b Corporative Research Centre for Forestry ^*  (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

bacterial carbon production; biogeochemistry; clearfell forestry; dissolved organic matter; fluorescence; headwater streams; PARAFAC

Indexed keywords

ALLOCHTHONY; BACTERIUM; BENTHOS; BIOGEOCHEMISTRY; CATCHMENT; CHEMICAL COMPOSITION; CLEARCUTTING; DISSOLVED ORGANIC MATTER; DISTURBANCE; HARVESTING; HEADWATER; LEAF AREA INDEX; OLD-GROWTH FOREST; STREAMWATER;

AUSTRALIA; TASMANIA;

BACTERIA (MICROORGANISMS);

EID: 84884335079     PISSN: 21619549     EISSN: 21619565     Source Type: Journal    
DOI: 10.1899/12-163.1     Document Type: Article

References (79)

1. AMON, R. M. W., AND R. BENNER. 1996. Bacterial utilization of different size classes of dissolved organic matter. Limnology and Oceanography 41:41-51.
2. APHA (AMERICAN PUBLIC HEALTH ASSOCIATION). 2005. Standard methods for the examination of water and wastewater. 21st edition. American Public Health Association, American Water Works Association, and Water Environment Federation, Washington, DC.
3. ASHTON, D. 1975. Studies of litter in Eucalyptus regnans forests. Australian Journal of Botany 23:413-433.
4. BERGGREN, M., H. LAUDON, AND M. JANSSON. 2009. Aging of allochthonous organic carbon regulates bacterial production in unproductive boreal lakes. Limnology and Oceanography 54:1333-1342.
5. BERTILSSON, S., AND J. N. JONES. 2003. Supply of dissolved organic matter to aquatic ecosystems: autochthonous sources. Pages 3-19 in S. E. G. Findlay and R. L. Sinsabaugh (editors). Aquatic ecosystems: interactivity of dissolved organic matter. Academic Press, Burlington, Massachusetts.
6. BIGGS, B. J. F., AND C. KILROY. 2000. Stream periphyton monitoring manual. National Institute of Water and Atmospheric Research for New Zealand Ministry for the Environment, Christchurch, New Zealand. (Available from: http://www.niwa.co.nz/our-science/freshwater/tools/periphyton)
7. BIRD, D. F., AND J. KALFF. 1984. Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Canadian Journal of Fisheries and Aquatic Sciences 41:1015-1023.
8. BLOTT, S. J., AND K. PYE. 2001. GRADISTAT: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surface Processes and Landforms 26:1237-1248.
9. BUESING, N., AND M. O. GESSNER. 2003. Incorporation of radiolabeled leucine into protein to estimate bacterial production in plant litter, sediment, epiphytic biofilms, and water samples. Microbial Ecology 45:291-301.
10. BUREAU OF METEOROLOGY. 2012. Tasmanian annual climate summary archive. Australian Government, Melbourne, Australia. (Available from: http://www.bom.gov.au/climate/current/annual/tas/archive/)
11. BURNHAM, K. P., AND D. R. ANDERSON. 2002. Model selection and multimodel inference: a practical informationtheoretic approach. Springer, New York.
12. CLAPCOTT, J. E. 2007. The metabolic signature of small headwater streams: natural variability and the response to forestry. PhD Thesis, University of Tasmania, Hobart, Australia.
13. CLAPCOTT, J. E., AND L. A. BARMUTA. 2009. Metabolic patch dynamics in small headwater streams: exploring spatial and temporal variability in benthic processes. Freshwater Biology 55:806-824.
14. CLAPCOTT, J. E., AND L. A. BARMUTA. 2010. Forest clearance increases metabolism and organic matter processes in small headwater streams. Journal of the North American Benthological Society 29:546-561.
15. COBLE, P. G. 1996. Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Marine Chemistry 51:325-346.
16. COLE, J. J. 1999. Aquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology. Ecosystems 2:215-225.
17. CORY, R. M., AND D. M. MCKNIGHT. 2005. Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter. Environmental Science and Technology 39:8142-8149.
18. CORY, R. M., M. P. MILLER, D. M. MCKNIGHT, J. J. GUERARD, AND P. L. MILLER. 2010. Effect of instrument-specific response on the analysis of fulvic acid fluorescence spectra. Limnology and Oceanography: Methods 8: 67-78.
19. DEL GIORGIO, P. A., AND M. L. PACE. 2008. Relative independence of dissolved organic carbon transport and processing in a large temperate river: the Hudson River as both pipe and reactor. Limnology and Oceanography 53:185-197.
20. DOCHERTY, K. M., K. C. YOUNG, P. A. MAURICE, AND S. D. BRIDGHAM. 2006. Dissolved organic matter concentration and quality influences upon structure and function of freshwater microbial communities. Microbial Ecology 52:378-388.
21. FELLMAN, J. B., D. V. D'AMORE, E. HOOD, AND R. D. BOONE. 2008. Fluorescence characteristics and biodegradability of dissolved organic matter in forest and wetland soils from coastal temperate watersheds in southeast Alaska. Biogeochemistry 88:169-184.
22. FELLMAN, J. B., E. HOOD, R. T. EDWARDS, AND D. V. D'AMORE. 2009. Changes in the concentration, biodegradability, and fluorescent properties of dissolved organic matter during stormflows in coastal temperate watersheds. Journal of Geophysical Research G: Biogeosciences 114. doi:10.1029/2008JG00790.
23. FELLMAN, J. B., E. HOOD, AND R. G. M. SPENCER. 2010. Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: a review. Limnology and Oceanography 55:2452-2462.
24. FINDLAY, S., J. M. QUINN, C. W. HICKEY, G. BURRELL, AND M. DOWNES. 2001. Effects of land use and riparian flowpath on delivery of dissolved organic carbon to streams. Limnology and Oceanography 46:345-355.
25. FINDLAY, S., AND R. L. SINSABAUGH. 1999. Unravelling the sources and bioavailability of dissolved organic matter in lotic aquatic ecosystems. Marine and Freshwater Research 50:781-790.
26. FINDLAY, S. E. G., R. L. SINSABAUGH, W. V. SOBCZAK, AND M. HOOSTAL. 2003. Metabolic and structural response of hyporheic microbial communities to variations in supply of dissolved organic matter. Limnology and Oceanography 48:1608-1617.
27. FISCHER, H., AND M. PUSCH. 1999. Use of the [14C]leucine incorporation technique to measure bacterial production in river sediments and the epiphyton. Applied and Environmental Microbiology 65:4411-4418.
28. FISCHER, H., AND M. PUSCH. 2001. Comparison of bacterial production in sediments, epiphyton and the pelagic zone of a lowland river. Freshwater Biology 46: 1335-1348.
29. FOREST PRACTICES BOARD. 2000. Forest Practices Code. Forest Practices Board, Hobart, Australia. (Available from: http://www.fpa.tas.gov.au/)
30. FRAZER, G. W., C. D. CANHAM, AND K. P. LERTZMAN. 1999. Gap Light Analyzer (GLA): imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Simon Fraser University, Burnaby, British Columbia, and the Institute of Ecosystem Studies, Millbrook, New York.
31. GUILLEMETTE, F., AND P. A. DEL GIORGIO. 2011. Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems. Limnology and Oceanography 56:734-748.
32. HICKEY, J. E., AND G. R. WILKINSON. 1999. The development and current implementation of silvicultural practices in native forests in Tasmania. Australian Forestry 62: 245-254.
33. HINTON, M. J., S. L. SCHIFF, AND M. C. ENGLISH. 1997. The significance of storms for the concentration and export of dissolved organic carbon from two Precambrian Shield catchments. Biogeochemistry 36:67-88.
34. HOEFFDING, W. 1948. A non-parametric test of independence. Annals of Mathematical Statistics 19:546-557.
35. HOLMES, R. M., J. W. MCCLELLAND, P. A. RAYMOND, B. B. FRAZER, B. J. PETERSON, AND M. STIEGLITZ. 2008. Lability of DOC transported by Alaskan rivers to the Arctic Ocean. Geophysical Research Letters 35 doi:10.1029/2007GL032837.
36. INAMDAR, S., N. FINGER, S. SINGH, M. MITCHELL, D. LEVIA, H. BAIS, D. SCOTT, AND P. MCHALE. 2011a. Dissolved organic matter (DOM) concentration and quality in a forested mid-Atlantic watershed, USA. Biogeochemistry 108: 55-76.
37. INAMDAR, S., S. SINGH, S. DUTTA, D. LEVIA, M. MITCHELL, D. SCOTT, H. BAIS, AND P. MCHALE. 2011b. Fluorescence characteristics and sources of dissolved organic matter for stream water during storm events in a forested mid-Atlantic watershed. Journal of Geophysical Research G: Biogeosciences 116. doi:10.1029/2011JG001735.
38. JAFFÉ, R., D. MCKNIGHT, N. MAIE, R. CORY, W. H. MCDOWELL, AND J. L. CAMPBELL. 2008. Spatial and temporal variations in DOM composition in ecosystems: the importance of long-term monitoring of optical properties. Journal of Geophysical Research G: Biogeosciences 113. doi:10. 1029/2008JG000683.
39. JANSSON, M., A. K. BERGSTRÖM, D. LYMER, K. VREDE, AND J. KARLSSON. 2006. Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microbial Ecology 52: 358-364.
40. JOHNSON, L. T., J. L. TANK, AND C. P. ARANGO. 2009. The effect of land use on dissolved organic carbon and nitrogen uptake in streams. Freshwater Biology 54:2335-2350.
41. JUDD, K. E., B. C. CRUMP, AND G. W. KLING. 2006. Variation in dissolved organic matter controls bacterial production and community composition. Ecology 87:2068-2079.
42. KAPLAN, L. A., AND T. L. BOTT. 1983. Microbial heterotrophic utilization of dissolved organic matter in a piedmont stream. Freshwater Biology 13:363-377.
43. KAPLAN, L. A., AND T. L. BOTT. 1989. Diel fluctuations in bacterial activity on streambed substrata during vernal algal blooms: effects of temperature, water chemistry, and habitat. Limnology and Oceanography 34:718-733.
44. KREUTZWEISER, D. P., K. P. GOOD, S. S. CAPELL, AND S. B. HOLMES. 2008. Leaf-litter decomposition and macroinvertebrate communities in boreal forest streams linked to upland logging disturbance. Journal of the North American Benthological Society 27:1-15.
45. KRITZBERG, E. S., J. J. COLE, M. L. PACE, W. GRANÉ LI, AND D. L. BADE. 2004. Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake 13C addition experiments. Limnology and Oceanography 49:588-596.
46. KRITZBERG, E. S., J. J. COLE, M. M. PACE, AND W. GRANÉ LI. 2005. Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs Aquatic Microbial Ecology 38:103-111.
47. LAFFAN, M. D. 2001. Geology and soils in the Warra LTER site: a preliminary description. Tasforests 13:23-29.
48. MARXSEN, J. 1996. Measurement of bacterial production in stream-bed sediments via leucine incorporation. FEMS Microbiology Ecology 21:313-325.
49. MCCALLISTER, S. L., J. E. BAUER, AND E. A. CANUEL. 2006. Bioreactivity of estuarine dissolved organic matter: a combined geochemical and microbiological approach. Limnology and Oceanography 51:94-100.
50. MCCALLISTER, S. L., J. E. BAUER, J. E. CHERRIER, AND H. W. DUCKLOW. 2004. Assessing sources and ages of organic matter supporting river and estuarine bacterial production: a multiple-isotope (d14C, d13C, and d15N) approach. Limnology and Oceanography 49:1687-1702.
51. MCKNIGHT, D. M., E. W. BOYER, P. K. WESTERHOFF, P. T. DORAN, T. KULBE, AND D. T. ANDERSON. 2001. Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnology and Oceanography 46:38-48.
52. MEYER, J. L., AND J. B. WALLACE. 2001. Lost linkages and lotic ecology: rediscovering small streams. Pages 295-317 in M. C. Press, N. J. Huntley, and S. A. Levin (editors). Ecology: achievement and challenge. Blackwell, Cornwall, UK.
53. MURPHY, K. R., G. M. RUIZ, W. T. M. DUNSMUIR, AND T. D. WAITE. 2006. Optimized parameters for fluorescencebased verification of ballast water exchange by ships. Environmental Science and Technology 40: 2357-2362.
54. NEPC (NATIONAL ENVIRONMENT PROTECTION COUNCIL). 1999. National Environment Protection (Assessment of Site Contamination) Measure: schedule B(3) guideline on laboratory analysis of potentially contaminated soils. National Environment Protection Council, Canberra, Australia.
55. OHNO, T. 2002. Fluorescence inner-filtering correction for determining the humification index of dissolved organic matter. Environmental Science and Technology 36: 742-746.
56. OLAPADE, O. A., AND L. G. LEFF. 2006. Influence of dissolved organic matter and inorganic nutrients on the biofilm bacterial community on artificial substrates in a northeastern Ohio, USA, stream. Canadian Journal of Microbiology 52:540-549.
57. POLLARD, P. C., AND H. DUCKLOW. 2011. Ultrahigh bacterial production in a eutrophic subtropical Australian river: does viral lysis short-circuit the microbial loop? Limnology and Oceanography 56:1115-1129.
58. QUINN, G. P., AND M. J. KEOUGH. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK.
59. REES, G. N., G. BEATTIE, P. M. BOWEN, AND B. T. HART. 2005. Heterotrophic bacterial production in the lower Murray River, south-eastern Australia. Marine and Freshwater Research 56:835-841.
60. REID, J. B., R. S. HILL, M. J. BROWN, AND M. J. HOVENDEN. 1999. Vegetation of Tasmania. Australian Biological Resources Study, Hobart, Tasmania.
61. RICH, P. M. 1990. Characterizing plant canopies with hemispherical photographs. Remote Sensing Reviews 5:13-29.
62. SAKAMAKI, T., AND J. S. RICHARDSON. 2011. Biogeochemical properties of fine particulate organic matter as an indicator of local and catchment impacts on forested streams. Journal of Applied Ecology 48:1462-1471.
63. SHARPLES, C. 1994. Landforms and geological sites of geoconservation significance in the Huon Forest District. Volume 2. Description. Forestry Tasmania, Hobart, Australia.
64. SMITH, E. M., AND Y. T. PRAIRIE. 2004. Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnology and Oceanography 49:137-147.
65. SPENCER, R. G. M., G. R. AIKEN, K. P. WICKLAND, R. G. STRIEGL, AND P. J. HERNES. 2008. Seasonal and spatial variability in dissolved organic matter quantity and composition from the Yukon River basin, Alaska. Global Biogeochemical Cycles 22. doi:10.1029/2008GB003231.
66. STEDMON, C. A., AND R. BRO. 2008. Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnology and Oceanography: Methods 6: 572-579.
67. STEDMON, C. A., AND S. MARKAGER. 2005. Resolving the variability in dissolved organic matter fluorescence in a temperate estuary and its catchment using PARAFAC analysis. Limnology and Oceanography 50:686-697.
68. STRAUSS, E. A., AND G. A. LAMBERTI. 2002. Effect of dissolved organic carbon quality on microbial decomposition and nitrification rates in stream sediments. Freshwater Biology 47:65-74.
69. THACKWAY, R., AND I. D. CRESSWELL. 1995. An interim biogeographic regionalisation for Australia: a framework for setting priorities in the National Reserves System Cooperative Program. Reserve System Unit, Australian Nature Conservation Agency, Canberra, Australia. (Available from: http://www.environment.gov.au/parks/nrs/science/bioregion-framework/ibra/).
70. WALSH, C. J., A. H. ROY, J. W. FEMINELLA, P. D. COTTINGHAM, P. M. GROFFMAN, AND R. P. MORGAN. 2005. The urban stream syndrome: current knowledge and the search for a cure. Journal of the North American Benthological Society 24: 706-723.
71. WEISHAAR, J. L., G. R. AIKEN, B. A. BERGAMASCHI, M. S. FRAM, R. FUJII, AND K. MOPPER. 2003. Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environmental Science and Technology 37:4702-4708.
72. WELLS, P., AND J. HICKEY. 1999. Wet sclerophyll, mixed and swamp forest. Pages 224-243 in J. B. Reid, R. S. Hill, M. J. Brown, and M. J. Hovenden (editors). Vegetation of Tasmania. Monotone Art Printers, Hobart, Australia.
73. WETZEL, R. G. 1992. Gradient-dominated ecosystems: sources and regulatory functions of dissolved organic matter in freshwater ecosystems. Hydrobiologia 229: 181-198.
74. WHITE, P. A., J. KALFF, J. B. RASMUSSEN, AND J. M. GASOL. 1991. The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microbial Ecology 21:99-118.
75. WICKLAND, K. P., J. C. NEFF, AND G. R. AIKEN. 2007. Dissolved organic carbon in Alaskan boreal forest: sources, chemical characteristics, and biodegradability. Ecosystems 10:1323-1340.
76. WILLIAMS, C. J., Y. YAMASHITA, H. F. WILSON, R. JAFFÉ, AND M. A. XENOPOULOS. 2010. Unraveling the role of land use and microbial activity in shaping dissolved organic matter characteristics in stream ecosystems. Limnology and Oceanography 55:1159-1171.
77. WIPFLI, M. S., J. S. RICHARDSON, AND R. J. NAIMAN. 2007. Ecological linkages between headwaters and downstream ecosystems: transport of organic matter, invertebrates, and wood down headwater channels. Journal of the American Water Resources Association 43: 72-85.
78. YAMASHITA, Y., B. D. KLOEPPEL, J. KNOEPP, G. L. ZAUSEN, AND R. JAFFÉ . 2011. Effects of watershed history on dissolved organic matter characteristics in headwater streams. Ecosystems 14:1110-1122.
79. YAMASHITA, Y., L. J. SCINTO, N. MAIE, AND R. JAFFÉ . 2010. Dissolved organic matter characteristics across a subtropical wetland's landscape: application of optical properties in the assessment of environmental dynamics. Ecosystems 13:1006-1019.